Abstract

New techniques have identified a wide range of organisms with the capacity to carry out biological nitrogen fixation (BNF)-greatly expanding our appreciation of the diversity and ubiquity of N fixers-but our understanding of the rates and controls of BNF at ecosystem and global scales has not advanced at the same pace. Nevertheless, determining rates and controls of BNF is crucial to placing anthropogenic changes to the N cycle in context, and to understanding, predicting and managing many aspects of global environmental change. Here, we estimate terrestrial BNF for a pre-industrial world by combining information on N fluxes with (15)N relative abundance data for terrestrial ecosystems. Our estimate is that pre-industrial N fixation was 58 (range of 40-100) Tg N fixed yr(-1); adding conservative assumptions for geological N reduces our best estimate to 44 Tg N yr(-1). This approach yields substantially lower estimates than most recent calculations; it suggests that the magnitude of human alternation of the N cycle is substantially larger than has been assumed.

Fungal endophyte communities reflect environmental structuring across a Hawaiian landscapePROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICAZimmerman, N. B., Vitousek, P. M.2012; 109 (32): 13022-13027

Abstract

We surveyed endophytic fungal communities in leaves of a single tree species (Metrosideros polymorpha) across wide environmental gradients (500-5,500 mm of rain/y; 10-22 °C mean annual temperature) spanning short geographic distances on Mauna Loa Volcano, Hawai'i. Using barcoded amplicon pyrosequencing at 13 sites (10 trees/site; 10 leaves/tree), we found very high levels of diversity within sites (a mean of 551 ± 134 taxonomic units per site). However, among-site diversity contributed even more than did within-site diversity to the overall richness of more than 4,200 taxonomic units observed in M. polymorpha, and this among-site variation in endophyte community composition correlated strongly with temperature and rainfall. These results are consistent with suggestions that foliar endophytic fungi are hyperdiverse. They further suggest that microbial diversity may be even greater than has been assumed and that broad-scale environmental controls such as temperature and rainfall can structure eukaryotic microbial diversity. Appropriately constrained study systems across strong environmental gradients present a useful means to understand the environmental factors that structure the diversity of microbial communities.

Abstract

Nutrient limitation to primary productivity and other biological processes is widespread in terrestrial ecosystems, and nitrogen (N) and phosphorus (P) are the most common limiting elements, both individually and in combination. Mechanisms that drive P limitation, and their interactions with the N cycle, have received less attention than mechanisms causing N limitation. We identify and discuss six mechanisms that could drive P limitation in terrestrial ecosystems. The best known of these is depletion-driven limitation, in which accumulated P losses during long-term soil and ecosystem development contribute to what Walker and Syers termed a "terminal steady state" of profound P depletion and limitation. The other mechanisms are soil barriers that prevent access to P; transactional limitation, in which weathering of P-containing minerals does not keep pace with the supply of other resources; low-P parent materials; P sinks; and anthropogenic changes that increase the supply of other resources (often N) relative to P. We distinguish proximate nutrient limitation (which occurs where additions of a nutrient stimulate biological processes, especially productivity) from ultimate nutrient limitation (where additions of a nutrient can transform ecosystems). Of the mechanisms that drive P limitation, we suggest that depletion, soil barriers, and low-P parent material often cause ultimate limitation because they control the ecosystem mass balance of P. Similarly, demand-independent losses and constraints to N fixation can control the ecosystem-level mass balance of N and cause it to be an ultimate limiting nutrient.

Abstract

We compared forest canopy heights and nitrogen concentrations in long-term research sites and in 2 x 2 km landscapes surrounding these sites along a substrate age gradient in the Hawaiian Islands. Both remote airborne and ground-based measurements were used to characterize processes that control landscape-level variation in canopy properties. We integrated a waveform light detection and ranging (LiDAR) system, a high-resolution imaging spectrometer, and a global positioning system/inertial measurement unit to provide highly resolved images of ground topography, canopy heights, and canopy nitrogen concentrations (1) within a circle 50 m in radius focused on a long-term study site in the center of each landscape; (2) for the entire 2 x 2 km landscape regardless of land cover; and (3) after stratification, for our target cover class, native-dominated vegetation on constructional geomorphic surfaces throughout each landscape. Remote measurements at all scales yielded the same overall patterns as did ground-based measurements in the long-term sites. The two younger landscapes supported taller trees than did older landscapes, while the two intermediate-aged landscapes had higher canopy nitrogen (N) concentrations than did either young or old landscapes. However, aircraft-based analyses detected substantial variability in canopy characteristics on the landscape level, even within the target cover class. Canopy heights were more heterogeneous on the older landscapes, with coefficients of variation increasing from 23-41% to 69-78% with increasing substrate age. This increasing heterogeneity was associated with a larger patch size of canopy turnover and with dominance of most secondary successional stands by the mat-forming fern Dicranopteris linearis in the older landscapes.

Abstract

Prior to European contact in 1778, Hawaiians developed intensive irrigated pondfield agricultural systems in windward Kohala, Hawai'i. We evaluated three potential sources of nutrients to windward systems that could have sustained intensive agriculture: (1) in situ weathering of primary and secondary minerals in upland soils; (2) rejuvenation of the supply of rock-derived nutrients on eroded slopes and in alluvium; and (3) transport of rock-derived nutrients to crops via irrigation water. Our results show that most windward soils are infertile and suggest that weathering of minerals within upland soils was insufficient to sustain intensive agriculture without substantial cultural inputs. Erosion enhances weathering and so increases nutrient supply, with soils of the largest alluvial valleys (>200 m deep) retaining 37% of calcium from parent material (compared to 2% in upland sites). However, soils of smaller valleys that also supported pre-contact agricultural systems are substantially less enriched. Isotopic 87Sr/86Sr analyses of stream water demonstrate that at low to moderate stream flow over 90% of dissolved strontium derives from weathering of basalt rather than deposition of atmospheric sources; most other dissolved cations also derive from basalt weathering. We calculate that irrigation water could have supplied approximately 200 kg ha(-1) yr(-1) of calcium to pondfield systems, nearly 100 times more than was supplied by weathering in soils on stable geomorphic surfaces. In effect, irrigation waters brought nutrients from rocks to the windward crops.

Abstract

We asked if element concentrations in ferns differ systematically from those in woody dicots in ways that could influence ecosystem properties and processes. Phylogenetically, ferns are deeply separated from angiosperms; for our analyses we additionally separated leptosporangiate ferns into polypod ferns, a monophyletic clade of ferns which radiated after the rise of angiosperms, and all other leptosporangiate (non-polypod) ferns. We sampled both non-polypod and polypod ferns on a natural fertility gradient and within fertilized and unfertilized plots in Hawaii, and compared our data with shrub and tree samples collected previously in the same plots. Non-polypod ferns in particular had low Ca concentrations under all conditions and less plasticity in their N and P stoichiometry than did polypod ferns or dicots. Polypod ferns were particularly rich in N and P, with low N:P ratios, and their stoichiometry varied substantially in response to differences in nutrient availability. Distinguishing between these two groups has the potential to be useful both in and out of Hawaii, as they have distinct properties which can affect ecosystem function. These differences could contribute to the widespread abundance of polypod ferns in an angiosperm-dominated world, and to patterns of nutrient cycling and limitation in sites where ferns are abundant.

Abstract

Dinitrogen (N(2)) fixation is widely recognized as an important process in controlling ecosystem responses to global environmental change, both today and in the past; however, significant discrepancies exist between theory and observations of patterns of N(2) fixation across major sectors of the land biosphere. A question remains as to why symbiotic N(2)-fixing plants are more abundant in vast areas of the tropics than in many of the mature forests that seem to be nitrogen-limited in the temperate and boreal zones. Here we present a unifying framework for terrestrial N(2) fixation that can explain the geographic occurrence of N(2) fixers across diverse biomes and at the global scale. By examining trade-offs inherent in plant carbon, nitrogen and phosphorus capture, we find a clear advantage to symbiotic N(2) fixers in phosphorus-limited tropical savannas and lowland tropical forests. The ability of N(2) fixers to invest nitrogen into phosphorus acquisition seems vital to sustained N(2) fixation in phosphorus-limited tropical ecosystems. In contrast, modern-day temperatures seem to constrain N(2) fixation rates and N(2)-fixing species from mature forests in the high latitudes. We propose that an analysis that couples biogeochemical cycling and biophysical mechanisms is sufficient to explain the principal geographical patterns of symbiotic N(2) fixation on land, thus providing a basis for predicting the response of nutrient-limited ecosystems to climate change and increasing atmospheric CO(2).

Abstract

Biological invasions contribute to global environmental change, but the dynamics and consequences of most invasions are difficult to assess at regional scales. We deployed an airborne remote sensing system that mapped the location and impacts of five highly invasive plant species across 221,875 ha of Hawaiian ecosystems, identifying four distinct ways that these species transform the three-dimensional (3D) structure of native rain forests. In lowland to montane forests, three invasive tree species replace native midcanopy and understory plants, whereas one understory invader excludes native species at the ground level. A fifth invasive nitrogen-fixing tree, in combination with a midcanopy alien tree, replaces native plants at all canopy levels in lowland forests. We conclude that this diverse array of alien plant species, each representing a different growth form or functional type, is changing the fundamental 3D structure of native Hawaiian rain forests. Our work also demonstrates how an airborne mapping strategy can identify and track the spread of certain invasive plant species, determine ecological consequences of their proliferation, and provide detailed geographic information to conservation and management efforts.

Development of a diverse epiphyte community in response to phosphorus fertilizationECOLOGY LETTERSBenner, J. W., Vitousek, P. M.2007; 10 (7): 628-636

Abstract

The role of terrestrial soil nutrient supply in determining the composition and productivity of epiphyte communities has been little investigated. In a montane Hawaiian rainforest, we documented dramatic increases in the abundance and species richness of canopy epiphytes in a forest that had been fertilized annually with phosphorus (P) for 15 years; there was no response in forest that had been fertilized with nitrogen (N) or other nutrients. The response of N-fixing lichens to P fertilization was particularly strong, although mosses and non-N-fixing lichens also increased in abundance and diversity. We show that enhancement of canopy P availability is the most likely factor driving the bloom in epiphytes. These results provide strong evidence that terrestrial soil fertility may structure epiphyte communities, and in particular that the abundance of N-fixing lichens--a functionally important epiphyte group--may be particularly sensitive to ecosystem P availability.

Abstract

No species can maximize growth, reproduction and competitive ability across all environments, so the success of invasive species is habitat-dependent. Nutrient-rich habitats often experience more invasion than resource-poor habitats, a pattern consistent with traits generally associated with successful invaders (high growth rates, early reproduction and many offspring). However, invaders do colonize resource-poor environments, and the mechanisms that allow their success in these systems are poorly understood. Traits associated with resource conservation are widespread among species adapted to resource-poor environments, and invasive species may succeed in low-resource environments by employing resource conservation traits such as high resource-use efficiency (RUE; carbon assimilation per unit of resource). We investigated RUE in invasive and native species from three habitats in Hawaii where light, water or nutrient availability was limiting to plant growth. Here we show that across multiple growth forms and broad taxonomic diversity invasive species were generally more efficient than native species at using limiting resources on short timescales and were similarly efficient when RUE measures were integrated over leaf lifespans. Our data challenge the idea that native species generally outperform invasive species under conditions of low resource availability, and suggest that managing resource levels is not always an effective strategy for invasive species control.

Business strategies for conservation on private lands: Koa forestry as a case studyPROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICAGoldstein, J. H., Daily, G. C., Friday, J. B., Matson, P. A., Naylor, R. A.2006; 103 (26): 10140-10145

Abstract

Innovative financial instruments are being created to reward conservation on private, working lands. Major design challenges remain, however, to make investments in biodiversity and ecosystem services economically attractive and commonplace. From a business perspective, three key financial barriers for advancing conservation land uses must frequently be addressed: high up-front costs, long time periods with no revenue, and high project risk due to long time horizons and uncertainty. We explored ways of overcoming these barriers on grazing lands in Hawaii by realizing a suite of timber and conservation revenue streams associated with their (partial) reforestation. We calculated the financial implications of alternative strategies, focusing on Acacia koa ("koa") forestry because of its high conservation and economic potential. Koa's timber value alone creates a viable investment (mean net present value = $453/acre), but its long time horizon and poor initial cash flow pose formidable challenges for landowners. At present, subsidy payments from a government conservation program targeting benefits for biodiversity, water quality, and soil erosion have the greatest potential to move landowners beyond the tipping point in favor of investments in koa forestry, particularly when combined with future timber harvest (mean net present value = $1,661/acre). Creating financial mechanisms to capture diverse ecosystem service values through time will broaden opportunities for conservation land uses. Governments, nongovernmental organizations, and private investors have roles to play in catalyzing this transition by developing new revenue streams that can reach a broad spectrum of landowners.

Abstract

We used strontium isotopes and analysis of foliar and soil nutrients to test whether erosion can rejuvenate the supply of rock-derived nutrients in the lowland tropical rain forest of La Selva, Costa Rica. We expected that these nutrients would be depleted from soils on stable surfaces, a result of over one million years of weathering in situ. In fact, trees and palms in all landscape positions derive a relatively high percentage (> or =40%) of their strontium from bedrock, rather than atmospheric, sources. The fraction that is rock-derived increases on slopes, but with no detectable effect on plant macronutrient concentrations. These results differ from those in a similar ecosystem on Kauai, Hawaii, where plants on uneroded surfaces derive almost all of their foliar Sr from atmospheric, rather than bedrock, sources. The results from La Selva challenge the assumption that tropical Oxisols in general have low nutrient inputs from bedrock, and support the hypothesis that erosion can increase the supply of these nutrients in lower landscape positions.

Ground-based and remotely sensed nutrient availability across a tropical landscapePROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICAPorder, S., Asner, G. P., Vitousek, P. M.2005; 102 (31): 10909-10912

Abstract

Tropical soils often are assumed to be highly weathered and thus nutrient-depleted, but this prediction applies primarily to geomorphically stable surfaces. Topography complicates the assumption of nutrient depletion, because erosion can enhance the supply of nutrients to tropical ecosystems. Consequently, understanding nutrient availability across landscapes requires a spatially explicit assessment of the relative strength of depletion and enhancement. We document the relationship between foliar nutrients and topographic position across a 20-km(2), 4- to 5-million-year-old eroded landscape in Kaua'i, Hawai'i, and use this relationship to build a bottom-up map of predicted nutrient availability across this landscape. Only approximately 17% of the landscape is nutrient-poor, mostly on stable uplands; nutrient availability on slopes and valley bottoms is much higher, in some cases similar to the most fertile montane forests in the Hawaiian Islands. This pattern was corroborated by top-down remote sensing of area-integrated canopy phosphorus concentrations.

Remote analysis of biological invasion and biogeochemical changePROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICAAsner, G. P., Vitousek, P. M.2005; 102 (12): 4383-4386

Abstract

We used airborne imaging spectroscopy and photon transport modeling to determine how biological invasion altered the chemistry of forest canopies across a Hawaiian montane rain forest landscape. The nitrogen-fixing tree Myrica faya doubled canopy nitrogen concentrations and water content as it replaced native forest, whereas the understory herb Hedychium gardnerianum reduced nitrogen concentrations in the forest overstory and substantially increased aboveground water content. This remote sensing approach indicates the geographic extent, intensity, and biogeochemical impacts of two distinct invaders; its wider application could enhance the role of remote sensing in ecosystem analysis and management.

Abstract

Although global changes can alter ecosystem nutrient dynamics indirectly as a result of their effects on plant litter quality, the interactive effects of global changes on plant litter remain largely unexplored in natural communities. We investigated the effects of elevated CO2, N deposition, warming and increased precipitation on the composition of organic compounds in plant litter in a fully-factorial experiment conducted in a California annual grassland. While lignin increased within functional groups under elevated CO2, this effect was attenuated by warming in grasses and by water additions in forbs. CO2-induced increases in lignin within functional groups also were counteracted by an increase in the relative biomass of forbs, which contained less lignin than grasses. Consequently, there was no net change in the overall lignin content of senesced tissue at the plot level under elevated CO2. Nitrate additions increased N in both grass and forb litter, although this effect was attenuated by water additions. Relative to changes in N within functional groups, changes in functional group dominance had a minor effect on overall litter N at the plot level. Nitrate additions had the strongest effect on decomposition, increasing lignin losses from Avena litter and interacting with water additions to increase decomposition of litter of other grasses. Increases in lignin that resulted from elevated CO2 had no effect on decomposition but elevated CO2 increased N losses from Avena litter. Overall, the interactions among elements of global change were as important as single-factor effects in influencing plant litter chemistry. However, with the exception of variation in N, litter quality had little influence on decomposition over the short term.

Abstract

We quantified variation in plant nutrient concentrations and provenance along catenas in landscapes of three different ages (0.15, 1.4, and 4.1 ma) in the Hawaiian Islands. Strontium (Sr) isotopes demonstrate that erosion provides a renewed source of rock-derived nutrients to slopes in landscapes of all ages, in some cases reversing a million years of ecosystem development in a distance of 100 m. However the effects of this input vary with landscape age. Plants on uneroded surfaces in a 0.15-ma landscape derive approximately 20% of their Sr from local bedrock (foliar 87Sr/86Sr approximately 0.7085), while on adjacent slopes this increases to approximately 80% (foliar 87Sr/86Sr approximately 0.7045). Despite this shift in provenance, foliar N and P do not vary systematically with slope position. Conversely, eroded slopes in a 4.1-ma landscape show smaller increases in rock-derived cations relative to stable uplands (foliar 87Sr/86Sr approximately 0.7075 vs 0.7090), but have >50% higher foliar N and P. These results demonstrate both that erosion can greatly increase nutrient availability in older landscapes, and that the ecological effects of erosion vary with landscape age. In addition, there can be as much biogeochemical variation on fine spatial scales in eroding landscapes as there is across millions of years of ecosystem development on stable surfaces.

Abstract

Physiological traits that contribute to the establishment and spread of invasive plant species could also have impacts on ecosystem processes. The traits prevalent in many invasive plants, such as high specific leaf areas, rapid growth rates, and elevated leaf nutrient concentrations, improve litter quality and should increase rates of decomposition and nutrient cycling. To test for these ecosystem impacts, we measured initial leaf litter properties, decomposition rates, and nutrient dynamics in 11 understory plants from the Hawaiian islands in control and nitrogen + phosphorus fertilized plots. These included five common native species, four of which were ferns, and six aggressive invasive species, including five angiosperms and one fern. We found a 50-fold variation in leaf litter decay rates, with natives decaying at rates of 0.2-2.3 year(-1) and invaders at 1.4-9.3 year(-1). This difference was driven by very low decomposition rates in native fern litter. Fertilization significantly increased the decay rates of leaf litter from two native and two invasive species. Most invasive litter types lost nitrogen and phosphorus more rapidly and in larger quantities than comparable native litter types. All litter types except three native ferns lost nitrogen after 100 days of decomposition, and all litter types except the most recalcitrant native ferns lost >50% of initial phosphorus by the end of the experiment (204-735 days). If invasive understory plants displace native species, nutrient cycling rates could increase dramatically due to rapid decomposition and nutrient release from invasive litter. Such changes are likely to cause a positive feedback to invasion in Hawai'i because many invasive plants thrive on nutrient-rich soils.

Abstract

Before European contact, Hawai'i supported large human populations in complex societies that were based on multiple pathways of intensive agriculture. We show that soils within a long-abandoned 60-square-kilometer dryland agricultural complex are substantially richer in bases and phosphorus than are those just outside it, and that this enrichment predated the establishment of intensive agriculture. Climate and soil fertility combined to constrain large dryland agricultural systems and the societies they supported to well-defined portions of just the younger islands within the Hawaiian archipelago; societies on the older islands were based on irrigated wetland agriculture. Similar processes may have influenced the dynamics of agricultural intensification across the tropics.

Abstract

Anthropogenic changes to the global N cycle are important in part because added N alters the composition, productivity, and other properties of many natural ecosystems substantially. Why does added N have such a large impact? Why is N in short supply in so many natural ecosystems? Processes that slow the cycling of N relative to other elements and processes that control ecosystem-level inputs and outputs of N could cause N supply to limit the dynamics of ecosystems. We discuss stoichiometric differences between terrestrial plants and other organisms, the abundance of protein-precipitating plant defenses, and the nature of the C-N bond in soil organic matter as factors that can slow N cycling. For inputs, the energetic costs of N fixation and their consequences, the supply of nutrients other than N, and preferential grazing on N-fixers all could constrain the abundance and/or activity of biological N-fixers. Together these processes drive and sustain N limitation in many natural terrestrial ecosystems.

Abstract

Interspecific variation in polyphenol production by plants has been interpreted in terms of defense against herbivores. Several recent lines of evidence suggest that polyphenols also influence the pools and fluxes of inorganic and organic soil nutrients. Such effects could have far-ranging consequences for nutrient competition among and between plants and microbes, and for ecosystem nutrient cycling and retention. The significance of polyphenols for nutrient cycling and plant productivity is still uncertain, but it could provide an alternative or complementary explanation for the variability in polyphenol production by plants.

Abstract

The articles in this volume illustrate that the Hawaiian islands are perhaps the most extraordinary living museum of evolution on the planet. However, Hawaii's value as a museum has diminished as the products of millions of years of evolutionary radiation have been lost to habitat destruction and biological invasions by exotic species. Human-caused habitat destruction can largely be controlled in parks and preserves, but exotic species do not respect park boundaries and can degrade native communities within protected areas. On the other hand, invasions by exotic species provide a dynamic laboratory of ecological processes at the same time as they erode the value of the evolutionary museum.